The perception of empty and filled time intervals by rats

In experiment 1, rats were trained in a within-subjects design to discriminate durations of a filled interval, and durations of an empty interval (an unfilled interval marked at the beginning and end by a 500 ms tone). Training and psychophysical testing was conducted with three sets of anchor durations. Rats made more long responses for filled than for empty intervals at signal durations greater than the geometric mean. In experiment 2, group same was trained similarly to the rats in experiment 1 with the ambient conditions (houselight illumination) remaining the same during the inter-trial interval and the empty intervals. Group different was trained with the houselight turned off during empty and filled intervals. The similarity of ambient conditions during the inter-trial interval and the empty intervals did not significantly affect timing. Filled intervals were timed more precisely and they were perceived as longer than empty intervals of the same duration. The psychophysical functions superimposed across anchor duration sets. These results are the first clear evidence of a filled interval illusion in rats, and they suggest that this difference may reflect a clock rate effect (greater for filled intervals) rather than a switch latency effect (slower for empty intervals).     

Differential effects of empty and filled intervals on duration estimation by pigeons: tests of an attention-sharing explanation

Pigeons were trained in a within-subjects design to discriminate durations of an empty interval and a filled interval. Even when different stimuli were used to mark empty intervals and to signal filled intervals, pigeons judged empty intervals to be longer than equal-length filled intervals. This timing difference was not a result of pigeons timing marker duration on empty interval trials. Increasing marker duration did not produce an overestimation of the empty time intervals. It was suggested that this timing difference could be due to a reduction in attention to temporal processing on filled interval trials when visual stimuli are used. Consistent with this hypothesis, it was found that empty intervals were judged longer than filled intervals when testing occurred in a darkened test room, but not when the test room was illuminated. In addition, no timing difference was observed when different auditory stimuli were used as markers for empty intervals and as signals for filled intervals.     

Rats' memory for event duration in delayed matching-to-sample with nonspatial comparison response alternatives

Previous research has suggested that using stationary and moving levers as nonspatial response alternatives can significantly enhance the speed of acquiring a temporal discrimination in rats. In Experiment 1, rats were trained to discriminate 2 and 8s of magazine light illumination by responding to either a stationary lever or a moving lever with a cue light illuminated above it. Rats learned to discriminate event durations at a high level of accuracy after 25 sessions of training. During subsequent delay tests, rats exhibited a strong choose-long bias, indicating that they were timing from the onset of the magazine light until the entry of levers into the chamber. This occurred regardless of whether intertrial intervals and delay intervals were dark or illuminated. On test trials in which the sample was omitted, rats responded as if the short sample had been presented. In Experiment 2, the rats received extensive training with dark and illuminated variable delay intervals (1-4 s). However, they continued to exhibit a tendency to time from the onset of the magazine light until entry of the levers into the chamber. Although the use of stationary/uncued and moving/cued levers as response alternatives enhanced the speed of acquisition of the event duration discrimination in rats, additional procedural modifications will be necessary to prevent rats from timing during the delay interval.     

Interstimulus interval as a discriminative stimulus: Evidence of the generality of a novel asymmetry in temporal discrimination learning

Three appetitive conditioning experiments with rats examined temporal discrimination learning within Pavlovian conditioning trials. In all experiments, the duration of a feature white noise stimulus signaled whether or not a subsequent 10-s target tone would be reinforced. In Experiment 1, the feature durations were 4 and 1 min. For one group of rats (Group 4+/1−), 4 min of noise signaled that the tone would be reinforced and 1 min of noise signaled that the tone would not be reinforced. A second group (Group 1+/4−) was trained with the reverse contingency. The results showed a clear asymmetry in temporal discrimination learning: rats trained with 4+/1− (Long+/Short−) learned the discrimination readily (responding more in the tone on reinforced than on nonreinforced trials), whereas rats trained with 1+/4− (Short+/Long) did not. In Experiment 2, the feature durations were shortened to 60 and 15 s. Due to strong excitatory conditioning of the 15-s feature, the reverse asymmetry was observed, with the Short+/Long− discrimination learned more readily than the Long+/Short− discrimination. However, Experiment 3 demonstrated that the original Long+/Short− advantage could be recovered while using 60− and 15-s feature durations if the excitatory conditioning of the feature was reduced by including nonreinforced feature trials. The results support previous research involving the timing of intertrial intervals and are consistent with the temporal elements hypothesis which holds that the passage of time is encoded as a series of hypothetical stimulus elements.     

Pigeons' memory for sequences of light flashes: reliance on temporal properties and evidence for delay interval/gap confusion

In Experiment 1, pigeons were trained to discriminate between sequences of two and four light flashes (illumination of the feeder). Retention functions obtained with dark delays exhibited a choose-many bias at a 1-s delay and a choose-few bias at delays of 4 and 8s. Retention functions obtained with illuminated delays only displayed a slight choose-few bias. In Experiment 2, additional birds were trained with the same sample sequences. However, the intertrial interval was illuminated by the houselight for Group Light, and it was dark for Group Dark. The acquisition data suggested that multiple temporal features of the light flash sequences controlled choice responding. For both groups, the retention functions were similar to those obtained in Experiment 1. In Experiment 3, baseline training with a 1-s dark delay eliminated the choose-many bias, but a significant choose-few bias at extended dark delays was still observed. Pigeons discriminate light flash sequences by relying on temporal properties of the sequence rather than using an event switch to count flashes. The biased-forgetting effects obtained in these studies appear to be primarily due to confusion between the delay interval and the gap between light flashes.     

The role of temporal generalization in a temporal discrimination task

Two experiments trained rats to discriminate two or three stimulus durations using a temporal discrimination task. A standard peak shift effect was observed when training was administered with short versus long signals in Experiment 1. Both discrimination accuracy scores and the generalization gradients revealed that shorter intervals were discriminated more accurately, which may be due to the scalar property of timing. In Experiment 2, three signals (short, medium, and long) were associated with three different responses, or two of the intervals were associated with one response (short and long or short and medium) and the other interval with a different response. Here, the short/medium versus long discrimination was learned most readily of the three tasks. The results of both experiments indicated a strong contribution of learning of individual durations combined with scalar generalization gradients, but Experiment 2 indicated that categorical encoding of durations may have also been operating.     

Do rats time filled and empty intervals of equal duration differently?

The goal was to determine whether rats time filled and empty intervals of equal duration differently. Each of five rats was trained for 50 sessions on an instrumental appetitive head entry procedure in which food was available (primed) every 120 s. On "empty" cycles, 30s prior to the next food prime, a 0.5-s pulse of white noise was presented. On "filled" cycles, 30s prior to the next food prime, white noise came on and stayed on until food was delivered. The two types of cycles were presented with equal probability. The results showed that the rats timed both the food-to-food interval and the stimulus-to-food interval. A comparison of the response gradients on filled and empty cycles following stimulus presentation showed better temporal discrimination on filled cycles. The results were modeled using a Packet theory of timing, with a linear averaging rule to combine the temporal information provided by the stimulus and food. The model fits to the individual response gradients were evaluated with a Turing test.     

Implicit, predictive timing draws upon the same scalar representation of time as explicit timing

It is not yet known whether the scalar properties of explicit timing are also displayed by more implicit, predictive forms of timing. We investigated whether performance in both explicit and predictive timing tasks conformed to the two psychophysical properties of scalar timing: the Psychophysical law and Weber's law. Our explicit temporal generalization task required overt estimation of the duration of an empty interval bounded by visual markers, whereas our temporal expectancy task presented visual stimuli at temporally predictable intervals, which facilitated motor preparation thus speeding target detection. The Psychophysical Law and Weber's Law were modeled, respectively, by (1) the functional dependence between mean subjective time and real time (2) the linearity of the relationship between timing variability and duration. Results showed that performance for predictive, as well as explicit, timing conformed to both psychophysical properties of interval timing. Both tasks showed the same linear relationship between subjective and real time, demonstrating that the same representational mechanism is engaged whether it is transferred into an overt estimate of duration or used to optimise sensorimotor behavior. Moreover, variability increased with increasing duration during both tasks, consistent with a scalar representation of time in both predictive and explicit timing. However, timing variability was greater during predictive timing, at least for durations greater than 200 msec, and ascribable to temporal, rather than non-temporal, mechanisms engaged by the task. These results suggest that although the same internal representation of time was used in both tasks, its external manifestation varied as a function of temporal task goals.     

Relative temporal representations in Pavlovian conditioning

The transfer of relative temporal representations was assessed in a series of three experiments. In each experiment, rats (Rattus norvegicus) received one set of conditioned stimulus (CS) and intertrial interval (ITI) durations in Phase 1 and another set in Phase 2. The ratio between the CS and ITI intervals was either changed or maintained across phases. On the hypothesis that relative temporal representations are learned, groups receiving maintained temporal ratios across phases were expected to display greater change in responding upon encountering the new intervals. When the CS duration decreased across phases, maintaining the temporal ratio did lead to greater change in Day 1 of Phase 2 towards the final pattern of responding. However, when the CS increased across phases, maintaining the temporal ratio across phases did not facilitate adjustment to the new intervals, suggesting that extinction of previously reinforced times induced new learning. These results provide evidence that under some conditions, relative relationships in temporal maps may survive transformation-of-scale, like relative relationships in spatial maps.     

Timing Rhythms: Perceived Duration Increases with a Predictable Temporal Structure of Short Interval Fillers

Variations in the temporal structure of an interval can lead to remarkable differences in perceived duration. For example, it has previously been shown that isochronous intervals, that is, intervals filled with temporally regular stimuli, are perceived to last longer than intervals left empty or filled with randomly timed stimuli. Characterizing the extent of such distortions is crucial to understanding how duration perception works. One account to explain effects of temporal structure is a non-linear accumulator-counter mechanism reset at the beginning of every subinterval. An alternative explanation based on entrainment to regular stimulation posits that the neural response to each filler stimulus in an isochronous sequence is amplified and a higher neural response may lead to an overestimation of duration. If entrainment is the key that generates response amplification and the distortions in perceived duration, then any form of predictability in the temporal structure of interval fillers should lead to the perception of an interval that lasts longer than a randomly filled one. The present experiments confirm that intervals filled with fully predictable rhythmically grouped stimuli lead to longer perceived duration than anisochronous intervals. No general over- or underestimation is registered for rhythmically grouped compared to isochronous intervals. However, we find that the number of stimuli in each group composing the rhythm also influences perceived duration. Implications of these findings for a non-linear clock model as well as a neural response magnitude account of perceived duration are discussed.     

Shifts in the psychophysical function in rats

The primary goal was to compare results from a free-operant procedure with pigeons [Machado, A., Guilhardi, P., 2000. Shifts in the psychometric function and their implications for models of timing. J. Exp. Anal. Behav. 74, 25-54, Experiment 2] with new results obtained with rats. The secondary goal was to compare the results of both experiments with dependent variables that were not used in the original publication. As in the original study with pigeons, rats were trained on a two-alternative free-operant psychophysical procedure in which left lever press responses were reinforced during the first and second quarters of a 60-s trial, and right lever press responses were reinforced during the third and fourth quarters of the trial. The quarters were reinforced according to four independent variable interval (VI) schedules of reinforcement. The VI duration was manipulated in each quarter, and shifts in the psychophysical functions that relate response rate with time since trial onset were measured. The results obtained with rats were consistent with those previously obtained with pigeons. In addition, results not originally reported were also consistent between rats and pigeons, and provided insights into the perception, memory, and decision processes in Scalar Expectancy Theory and Learning-to-Time Theory.     

Temporal discrimination in a long operant chamber

Pigeons were placed in a long chamber equipped with one key and feeder at each end side and one key and houselight at the middle. To obtain food the birds had to choose one side key after a short signal and the other side key after a long signal. The signals consisted of the illumination of the center key and the houselight and were initiated by a peck at the center key. The chamber had sensitive floor panels that enabled us to measure the location of the bird during the signals. In Experiment 1, after the birds learned the discrimination we reversed the assignment of keys to signals. In Experiment 2, we examined performance on two pairs of discriminations holding the same ratio. In Experiment 3, after the pigeons learned to discriminate two signals, we changed the duration of the long signal. The results showed that (a) the birds' motion during the signal was highly stereotypical, i.e. the birds moved to the short side, waited a few seconds, and then departed to, and stayed on the long side; (b) this motion pattern predicted the results of generalization tests with novel durations; (c) the mean of the times of departure from the short side approached its steady state values quicker than the standard deviation and consequently superposition of behavioral measures became stronger with training; (d) only the duration of the short signal influenced significantly the moment the birds departed from the short side; finally (e) the times of arrival at and departure from the short side were positively correlated, but the times of arrival and residence at the short side were negatively correlated.     

Effect of training delays and start and stop markers on the choose-short effect in pigeons

Pigeons were trained in a matching-to-duration task using short and long filled intervals. Group 2/8 was trained with 2- and 8-s intervals, Group 4/10 with 4- and 10-s intervals, and group marker with 2- and 8-s intervals presented between 1-s start and stop markers. Extended-delay testing showed no significant choose-short effect (CSE) in any group. It was hypothesized that the lack of a CSE may have resulted from use of a variable delay (range 1-3s) during training. The same subjects were employed in Experiment 2 and were trained with a new set of comparisons and one of the alternate types of samples employed in Experiment 1. All training trials involved a 0-s delay. Extended-delay testing revealed a significant CSE in Groups 2/8 and 4/10 but only a weak, and statistically nonsignificant, CSE in group marker. It was concluded that use of a variable delay during training reduced the CSE. The notion that subjective shortening underlies the CSE provided an adequate account of these findings.     

Interval timing by an invertebrate, the bumble bee Bombus impatiens

Sensitivity to temporal information and the ability to adjust behavior to the temporal structure of the environment should be phylogenetically widespread. Some timing abilities, such as sensitivity to circadian cycles, appear in a wide range of invertebrate and vertebrate taxa [1,2]. Interval timing--sensitivity to the duration of time intervals--has, however, only been shown to occur in vertebrates [3,4]. Insect pollinators make a variety of decisions that would appear to require the ability to estimate elapsed durations. We exposed bumble bees to conditions in which proboscis extension was reinforced after a fixed duration had elapsed or after either of two fixed durations had elapsed. Two groups of bees were trained with a short duration (either 6 s or 12 s) and a long duration (36 s) in separate experimental phases (independent timing groups), whereas two other groups were trained with a short duration (either 6 s or 12 s) and long duration (36 s) always intermixed unpredictably (multiple timing groups). On long intervals, independent timing groups waited longer than mixed timing groups to generate the first response and responded maximally near the end of the interval. Multiple timing groups waited the same amount of time on average before generating the first response on both long and short intervals. On individual trials, multiple timing groups appeared to time either the long duration only or both the short and long durations: most trials were characterized by a single burst of responding that began between the short and long duration values or by two bursts of responding with the first burst bracketing the short value and the second burst beginning in anticipation of the long value. These results show that bumble bees learn to time interval durations and can flexibly time multiple durations simultaneously. The results indicate no phylogenetic divide between vertebrates and invertebrates in interval timing ability.     

Relevance of a neutral cue in a two-choice detection task in the rat

Relevance of a neutral cue for performance in a two-choice visuospatial detection task was examined. Nine rats were trained, 5 with short intertrial interval (ITI) and 4 with long ITI, to detect a target (lateral lights) presented after a neutral-cue (central light). The removal of the neutral-cue decreased accuracy and increased response latencies and omissions. These results demonstrate that a neutral-cue, preceding the target, is relevant for the performance, suggesting that rats are highly expectant during the neutral-cue and reallocate attentional resources during ITI. Furthermore, latencies were higher, omissions were lower and the fall of accuracy was greater for rats with long than with short ITI, which could indicate that the neutral-cue was more relevant for the former group.     

Serial conditional discrimination and temporal bisection in rats selectively lesioned in the dentate gyrus

In positive serial conditional discrimination, animals respond during a target stimulus when it is preceded by a feature stimulus, but they do not respond when the same target stimulus is presented alone. Moreover, the feature and target stimuli are separated from each other by an empty interval. The present work aimed to investigate if two durations (4 or 16 s) of the same feature stimulus (light) could modulate the operant responses of rats to different levers (A and B) during a 5-s target stimulus (tone). In the present study, lever A was associated with the 4-s light, and lever B was associated with the 16-s light. A 5-s empty interval was included between the light and the tone. In the same training procedure, the rats were also presented with the 5-s tone without the preceding light stimuli. In these trials, the responses were not reinforced. We evaluated the hippocampal involvement of these behavioral processes by selectively lesioning the dentate gyrus with colchicine. Once trained, the rats were submitted to a test using probe trials without reinforcement. They were presented with intermediate durations of the feature stimulus (light) to obtain a temporal bisection curve recorded during the exposure to the target stimuli. The rats from both groups learned to respond with high rates during tones preceded by light and with low rates during tones presented alone, which indicated acquisition of the serial conditional discrimination. The rats were able to discriminate between the 4- and 16-s lights by correctly choosing lever A or B. In the test, the temporal bisection curves from both experimental groups showed a bisection point at the arithmetic mean between 4 and 16 s. Such processes were not impaired by the dentate gyrus lesion. Thus, our results showed that different durations of a feature stimulus could result in conditional properties. However, this processing did not appear to depend on the dentate gyrus alone.     

Temporal discrimination learning by pigeons

Memory for time by animals appears to undergo a systematic shortening. This so-called choose-short effect can be seen in a conditional temporal discrimination when a delay is inserted between the sample and comparison stimuli. We have proposed that this temporal shortening may result from a procedural artifact in which the delay appears similar to the intertrial interval and thus, produces an inadvertent ambiguity or 'instructional failure'. When this ambiguity is avoided by distinguishing the intertrial interval from the delay, as well as the samples from the delay, the temporal shortening effect and other asymmetries often disappear. By avoiding artifacts that can lead to a misinterpretation of results, we may understand better how animals represent time. An alternative procedure for studying temporal discriminations is with the psychophysical bisection procedure in which following conditional discrimination training, intermediate durations are presented and the point of subjective equality is determined. Research using the bisection procedure has shown that pigeons represent temporal durations not only as their absolute value but also relative to durations from which they must be discriminated. Using this procedure, we have also found that time passes subjectively slower when animals are required to respond to the to-be-timed stimulus.     

Responding maintained by primary reinforcing visual stimuli is increased by nicotine administration in rats

Nicotine has been shown to increase responding maintained by turning off a houselight. To examine whether this effect extends to other primary reinforcing visual stimuli, the present study assessed whether nicotine would increase responding maintained by the illumination, and not just the darkening, of a visual stimulus. One group of rats (n = 4) was initially trained to press two levers, using food as a consequence, while a separate group of rats (n = 4) was initially trained to press one lever. After training, all rats pressed an active lever to turn on or turn off a houselight for 10 s, while presses on an inactive lever had no programmed consequences. A third group of rats (n = 4) were never trained to press either of the two levers and did not experience any programmed consequences for pressing. Although nicotine slightly increased lever pressing on both levers in the third group, nicotine resulted in much greater increases in responding maintained by the visual stimuli in the first two groups. Nicotine selectively increased responding maintained by visual stimuli, regardless of which levers were originally trained and regardless of whether those stimuli consisted of turning on or turning off a houselight, suggesting that nicotine enhances the value of primary reinforcing visual stimuli.     

Timescale dependence in a conditional temporal discrimination procedure

A conditional temporal discrimination procedure was used to test the scope and generality of the principle of timescale invariance (TSI). Rats were trained to make different temporal discriminations following four different auditory stimuli. After shorter stimuli, rats were reinforced for pressing the left lever, and after longer stimuli, rats were reinforced for pressing the right lever. The four auditory stimuli (a pure tone, pulsed tone, click, and white noise) were each presented for different pairs of durations (ranging from 2 vs. 8s to 32 vs. 128 s) within a single session, but the ratio between the shorter and longer duration was maintained constant at 1:4. With the shortest pair of durations (2 vs. 8s), rats showed a clear violation of TSI in both overall and relative response rates. Rats started responding later and persisted relatively longer on the left lever when the shorter duration was only 2s. We interpret these results with regards to a framing hypothesis, whereby TSI does not apply to relatively short durations when animals are simultaneously trained with wide ranges of intervals.     

Pair comparison of durations

Pigeons were trained on a pair comparison task where a red light of one duration was followed by a green light of a second duration. Following a duration pair two choice keys were lit and one choice was reinforced if the duration of red was longer than green, and the alternate choice was reinforced if green was longer than red. Duration pairs consisted of all possible combinations of the durations .5, 1, 2, and 4 sec in one condition, and 2, 4, 8, and 16 sec in a second condition. Generalization tests with novel duration pairs were given under both conditions. Under a final set of conditions, interstimulus intervals of 2, 5, 10, and 30 sec were interposed between the first (red) and second (green) durations. Pigeons responded appropriately in most cases, with accuracy a function of the relative temporal difference between the members of a duration pair. Accuracy on transfer problems was above 70% in most instances, but in some cases suggests factors apart from relative temporal differences influenced performance. Accuracy declined with increases in the interstimulus interval, but remained above chance levels even when the longest interstimulus interval was used.